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Published in: BMC Neurology 1/2014

Open Access 01-12-2014 | Research article

Effects of minimally invasive procedures for evacuation of intracerebral hematoma in early stages on MMP-9 and BBB permeability in rabbits

Authors: Guofeng Wu, Jing Shi, Fan Wang, Likun Wang, Anrong Feng, Siying Ren

Published in: BMC Neurology | Issue 1/2014

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Abstract

Background

The effects of performing a minimally invasive procedure at different stages after intracerebral hemorrhage on perihematomal MMP-9 expression and blood–brain barrier (BBB) permeability were evaluated.

Methods

Sixty rabbits were randomly distributed into a model control group (MC group, 30 rabbits) or a minimally invasive group (MI group, 30 rabbits). A model of intracerebral hemorrhage was established in the MC and MI group. In the MI group, the intracerebral hematoma was evacuated by stereotactic minimally invasive procedures over 6 hours (6 rabbits), 12 hours (6 rabbits), 18 hours (6 rabbits) 24 hours or 48 hours (6 rabbits) following successful induction of intracerebral hemorrhage. The same procedure was performed in the MC group at the same time point but without evacuating the hematoma. All the animals were sacrificed within two weeks after the hematoma was surgically evacuated. A neurological deficit score was determined, and the perihematomal MMP-9 level and the BBB permeability were measured.

Results

The neurological deficit score, perihematomal MMP-9 level and BBB permeability of the MI group decreased significantly compared to the MC group. Performing the MI procedure 6–12 h after intracerebral hemorrhage showed the most favorable outcome.

Conclusions

Regarding the pathophysiological changes surrounding the hematoma, the optimal time window of performing MI procedures for the intracerebral hematoma evacuation might be within 6–12 h after hemorrhage.
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Literature
1.
go back to reference Rincon F, Mayer SA: Current treatment options for intracerebral hemorrhage. Curr Treat Options Cardiovasc Med. 2008, 10 (3): 229-240.CrossRefPubMed Rincon F, Mayer SA: Current treatment options for intracerebral hemorrhage. Curr Treat Options Cardiovasc Med. 2008, 10 (3): 229-240.CrossRefPubMed
2.
go back to reference Miller CM, Vespa P, Saver JL, Kidwell CS, Carmichael ST, Alger J, Frazee J, Starkman S, Liebeskind D, Nenov V, Elashoff R, Martin N: Image-guided endoscopic evacuation of spontaneous intracerebral hemorrhage. Surg Neurol. 2008, 69 (5): 441-446. discussion 446CrossRefPubMedPubMedCentral Miller CM, Vespa P, Saver JL, Kidwell CS, Carmichael ST, Alger J, Frazee J, Starkman S, Liebeskind D, Nenov V, Elashoff R, Martin N: Image-guided endoscopic evacuation of spontaneous intracerebral hemorrhage. Surg Neurol. 2008, 69 (5): 441-446. discussion 446CrossRefPubMedPubMedCentral
3.
go back to reference Orakcioglu B, Uozumi Y, Unterberg A: Endoscopic intra-hematomal evacuation of intracerebral hematomas - a suitable technique for patients with coagulopathies. Acta Neurochir. 2011, 112: 3-8.CrossRef Orakcioglu B, Uozumi Y, Unterberg A: Endoscopic intra-hematomal evacuation of intracerebral hematomas - a suitable technique for patients with coagulopathies. Acta Neurochir. 2011, 112: 3-8.CrossRef
4.
go back to reference Zhou H, Zhang Y, Liu L, Huang Y, Tang Y, Su J, Hua W, Han X, Xue J, Dong Q: Minimally invasive stereotactic puncture and thrombolysis therapy improves long-term outcome after acute intracerebral hemorrhage. J Neurol. 2011, 258 (4): 661-669.CrossRefPubMedPubMedCentral Zhou H, Zhang Y, Liu L, Huang Y, Tang Y, Su J, Hua W, Han X, Xue J, Dong Q: Minimally invasive stereotactic puncture and thrombolysis therapy improves long-term outcome after acute intracerebral hemorrhage. J Neurol. 2011, 258 (4): 661-669.CrossRefPubMedPubMedCentral
5.
go back to reference Zuccarello M, Andaluz N, Wagner KR: Minimally invasive therapy for intracerebral hematomas. Neurosurg Clin N Am. 2002, 13 (3): 349-354.CrossRefPubMed Zuccarello M, Andaluz N, Wagner KR: Minimally invasive therapy for intracerebral hematomas. Neurosurg Clin N Am. 2002, 13 (3): 349-354.CrossRefPubMed
6.
go back to reference Xu F, Tang Z, Luo X, Kang H, Hu Q, Wang W, Zhu S: No evidence of preoperative hematoma growth representing an increased postoperative rebleeding risk for minimally invasive aspiration and thrombolysis of ICH. Br J Neurosurg. 2010, 24 (3): 268-274.CrossRefPubMed Xu F, Tang Z, Luo X, Kang H, Hu Q, Wang W, Zhu S: No evidence of preoperative hematoma growth representing an increased postoperative rebleeding risk for minimally invasive aspiration and thrombolysis of ICH. Br J Neurosurg. 2010, 24 (3): 268-274.CrossRefPubMed
7.
go back to reference Barrett RJ, Hussain R, Coplin WM, Berry S, Keyl PM, Hanley DF, Johnson RR, Carhuapoma JR: Frameless stereotactic aspiration and thrombolysis of spontaneous intracerebral hemorrhage. Neurocrit Care. 2005, 3 (3): 237-245.CrossRefPubMed Barrett RJ, Hussain R, Coplin WM, Berry S, Keyl PM, Hanley DF, Johnson RR, Carhuapoma JR: Frameless stereotactic aspiration and thrombolysis of spontaneous intracerebral hemorrhage. Neurocrit Care. 2005, 3 (3): 237-245.CrossRefPubMed
8.
go back to reference Sun H, Liu H, Li D, Liu L, Yang J, Wang W: An effective treatment for cerebral hemorrhage: minimally invasive craniopuncture combined with urokinase infusion therapy. Neurol Res. 2010, 32 (4): 371-377.CrossRefPubMed Sun H, Liu H, Li D, Liu L, Yang J, Wang W: An effective treatment for cerebral hemorrhage: minimally invasive craniopuncture combined with urokinase infusion therapy. Neurol Res. 2010, 32 (4): 371-377.CrossRefPubMed
9.
go back to reference Miller CM, Vespa PM, McArthur DL, Hirt D, Etchepare M: Frameless stereotactic aspiration and thrombolysis of deep intracerebral hemorrhage is associated with reduced levels of extracellular cerebral glutamate and unchanged lactate pyruvate ratios. Neurocrit Care. 2007, 6 (1): 22-29.CrossRefPubMed Miller CM, Vespa PM, McArthur DL, Hirt D, Etchepare M: Frameless stereotactic aspiration and thrombolysis of deep intracerebral hemorrhage is associated with reduced levels of extracellular cerebral glutamate and unchanged lactate pyruvate ratios. Neurocrit Care. 2007, 6 (1): 22-29.CrossRefPubMed
10.
go back to reference Wu G, Wang L, Hong Z, Li C, Long X, Sheng F: Effects of minimally invasive procedures for removal of intracranial hematoma on matrix metalloproteinase expression and blood–brain barrier permeability in perihematomal brain tissues. Neurol Res. 2011, 33 (3): 300-306.CrossRefPubMed Wu G, Wang L, Hong Z, Li C, Long X, Sheng F: Effects of minimally invasive procedures for removal of intracranial hematoma on matrix metalloproteinase expression and blood–brain barrier permeability in perihematomal brain tissues. Neurol Res. 2011, 33 (3): 300-306.CrossRefPubMed
11.
go back to reference Wu G, Wang L, Hong Z, Mao Y, Hu X: Effects of minimally invasive techniques for evacuation of hematoma in basal ganglia on cortical spinal tract from patients with spontaneous hemorrhage: observed by diffusion tensor imaging. Neurol Res. 2010, 32 (10): 1103-1109.CrossRefPubMed Wu G, Wang L, Hong Z, Mao Y, Hu X: Effects of minimally invasive techniques for evacuation of hematoma in basal ganglia on cortical spinal tract from patients with spontaneous hemorrhage: observed by diffusion tensor imaging. Neurol Res. 2010, 32 (10): 1103-1109.CrossRefPubMed
12.
go back to reference Wang YF, Wu JS, Mao Y, Chen XC, Zhou LF, Zhang Y: The optimal time-window for surgical treatment of spontaneous intracerebral hemorrhage: result of prospective randomized controlled trial of 500 cases. Acta Neurochir. 2008, 105: 141-145.CrossRef Wang YF, Wu JS, Mao Y, Chen XC, Zhou LF, Zhang Y: The optimal time-window for surgical treatment of spontaneous intracerebral hemorrhage: result of prospective randomized controlled trial of 500 cases. Acta Neurochir. 2008, 105: 141-145.CrossRef
13.
go back to reference Keep RF, Xiang J, Ennis SR, Andjelkovic A, Hua Y, Xi G, Hoff JT: Blood–brain barrier function in intracerebral hemorrhage. Acta Neurochir. 2008, 105: 73-77.CrossRef Keep RF, Xiang J, Ennis SR, Andjelkovic A, Hua Y, Xi G, Hoff JT: Blood–brain barrier function in intracerebral hemorrhage. Acta Neurochir. 2008, 105: 73-77.CrossRef
14.
go back to reference Wu G, Wang L, Liu J, Mao Y, Qin G: Minimally Invasive Procedures Reduced the Damages to Motor Function in Patients with Thalamic Hematoma: Observed by Motor Evoked Potential and Diffusion Tensor Imaging. J Stroke Cerebrovasc Dis. 2013, 22 (3): 232-240.CrossRefPubMed Wu G, Wang L, Liu J, Mao Y, Qin G: Minimally Invasive Procedures Reduced the Damages to Motor Function in Patients with Thalamic Hematoma: Observed by Motor Evoked Potential and Diffusion Tensor Imaging. J Stroke Cerebrovasc Dis. 2013, 22 (3): 232-240.CrossRefPubMed
15.
go back to reference Hazell AS: Excitotoxic mechanisms in stroke: an update of concepts and treatment strategies. Neurochem Int. 2007, 50 (7–8): 941-953.CrossRefPubMed Hazell AS: Excitotoxic mechanisms in stroke: an update of concepts and treatment strategies. Neurochem Int. 2007, 50 (7–8): 941-953.CrossRefPubMed
16.
go back to reference Kawakita K, Kawai N, Kuroda Y, Yasashita S, Nagao S: Expression of matrix metalloproteinase-9 in thrombin-induced brain edema formation in rats. J Stroke Cerebrovasc Dis. 2006, 15 (3): 88-95.CrossRefPubMed Kawakita K, Kawai N, Kuroda Y, Yasashita S, Nagao S: Expression of matrix metalloproteinase-9 in thrombin-induced brain edema formation in rats. J Stroke Cerebrovasc Dis. 2006, 15 (3): 88-95.CrossRefPubMed
17.
go back to reference Wu CH, Huang FY, Wang KY, Huang SY, Yang RL, Li HZ, Lei HX, Lin JS, Wang JM, Yan XH: [Expression of matrix metalloproteinase MMP-9 in the plasma and hematoma fluid of intracerebral hemorrhage patients]. Zhonghua Yi Xue Za Zhi. 2008, 88 (3): 174-176.PubMed Wu CH, Huang FY, Wang KY, Huang SY, Yang RL, Li HZ, Lei HX, Lin JS, Wang JM, Yan XH: [Expression of matrix metalloproteinase MMP-9 in the plasma and hematoma fluid of intracerebral hemorrhage patients]. Zhonghua Yi Xue Za Zhi. 2008, 88 (3): 174-176.PubMed
18.
go back to reference Xue M, Fan Y, Liu S, Zygun DA, Demchuk A, Yong VW: Contributions of multiple proteases to neurotoxicity in a mouse model of intracerebral haemorrhage. Brain. 2009, 132 (Pt 1): 26-36.PubMed Xue M, Fan Y, Liu S, Zygun DA, Demchuk A, Yong VW: Contributions of multiple proteases to neurotoxicity in a mouse model of intracerebral haemorrhage. Brain. 2009, 132 (Pt 1): 26-36.PubMed
19.
go back to reference Xue M, Yong VW: Matrix metalloproteinases in intracerebral hemorrhage. Neurol Res. 2008, 30 (8): 775-782.CrossRefPubMed Xue M, Yong VW: Matrix metalloproteinases in intracerebral hemorrhage. Neurol Res. 2008, 30 (8): 775-782.CrossRefPubMed
20.
go back to reference Florczak-Rzepka M, Grond-Ginsbach C, Montaner J, Steiner T: Matrix metalloproteinases in human spontaneous intracerebral hemorrhage: an update. Cerebrovasc Dis. 2012, 34 (4): 249-262.CrossRefPubMed Florczak-Rzepka M, Grond-Ginsbach C, Montaner J, Steiner T: Matrix metalloproteinases in human spontaneous intracerebral hemorrhage: an update. Cerebrovasc Dis. 2012, 34 (4): 249-262.CrossRefPubMed
21.
go back to reference Wu G, Li C, Wang L, Mao Y, Hong Z: Minimally invasive procedures for evacuation of intracerebral hemorrhage reduces perihematomal glutamate content, blood–brain barrier permeability and brain edema in rabbits. Neurocrit Care. 2011, 14 (1): 118-126.CrossRefPubMed Wu G, Li C, Wang L, Mao Y, Hong Z: Minimally invasive procedures for evacuation of intracerebral hemorrhage reduces perihematomal glutamate content, blood–brain barrier permeability and brain edema in rabbits. Neurocrit Care. 2011, 14 (1): 118-126.CrossRefPubMed
22.
go back to reference Wu G, Sheng F, Wang L, Wang F: The pathophysiological time window study of performing minimally invasive procedures for the intracerebral hematoma evacuation in rabbit. Brain Res. 2012, 1465: 57-65.CrossRefPubMed Wu G, Sheng F, Wang L, Wang F: The pathophysiological time window study of performing minimally invasive procedures for the intracerebral hematoma evacuation in rabbit. Brain Res. 2012, 1465: 57-65.CrossRefPubMed
23.
go back to reference Purdy PD, Devous MD, Batjer HH, White CL, Meyer Y, Samson DS: Microfibrillar collagen model of canine cerebral infarction. Stroke. 1989, 20 (10): 1361-1367.CrossRefPubMed Purdy PD, Devous MD, Batjer HH, White CL, Meyer Y, Samson DS: Microfibrillar collagen model of canine cerebral infarction. Stroke. 1989, 20 (10): 1361-1367.CrossRefPubMed
24.
go back to reference Xi G, Keep RF, Hua Y, Xiang J, Hoff JT: Attenuation of thrombin-induced brain edema by cerebral thrombin preconditioning. Stroke. 1999, 30 (6): 1247-1255.CrossRefPubMed Xi G, Keep RF, Hua Y, Xiang J, Hoff JT: Attenuation of thrombin-induced brain edema by cerebral thrombin preconditioning. Stroke. 1999, 30 (6): 1247-1255.CrossRefPubMed
25.
go back to reference Adeoye O, Broderick JP: Advances in the management of intracerebral hemorrhage. Nat Rev. 2010, 6 (11): 593-601. Adeoye O, Broderick JP: Advances in the management of intracerebral hemorrhage. Nat Rev. 2010, 6 (11): 593-601.
26.
go back to reference Xue M, Hollenberg MD, Demchuk A, Yong VW: Relative importance of proteinase-activated receptor-1 versus matrix metalloproteinases in intracerebral hemorrhage-mediated neurotoxicity in mice. Stroke. 2009, 40 (6): 2199-2204.CrossRefPubMed Xue M, Hollenberg MD, Demchuk A, Yong VW: Relative importance of proteinase-activated receptor-1 versus matrix metalloproteinases in intracerebral hemorrhage-mediated neurotoxicity in mice. Stroke. 2009, 40 (6): 2199-2204.CrossRefPubMed
27.
go back to reference Hernandez-Guillamon M, Martinez-Saez E, Delgado P, Domingues-Montanari S, Boada C, Penalba A, Boada M, Pagola J, Maisterra O, Rodriguez-Luna D, Molina CA, Rovira A, Alvarez-Sabin J, Ortega-Aznar A, Montaner J: MMP-2/MMP-9 plasma level and brain expression in cerebral amyloid angiopathy-associated hemorrhagic stroke. Brain Pathol. 2012, 22 (2): 133-141.CrossRefPubMed Hernandez-Guillamon M, Martinez-Saez E, Delgado P, Domingues-Montanari S, Boada C, Penalba A, Boada M, Pagola J, Maisterra O, Rodriguez-Luna D, Molina CA, Rovira A, Alvarez-Sabin J, Ortega-Aznar A, Montaner J: MMP-2/MMP-9 plasma level and brain expression in cerebral amyloid angiopathy-associated hemorrhagic stroke. Brain Pathol. 2012, 22 (2): 133-141.CrossRefPubMed
28.
go back to reference Koh SH, Park CY, Kim MK, Lee KY, Kim J, Chang DI, Kim HT, Kim SH: Microbleeds and free active MMP-9 are independent risk factors for neurological deterioration in acute lacunar stroke. Eur J Neurol. 2011, 18 (1): 158-164.CrossRefPubMed Koh SH, Park CY, Kim MK, Lee KY, Kim J, Chang DI, Kim HT, Kim SH: Microbleeds and free active MMP-9 are independent risk factors for neurological deterioration in acute lacunar stroke. Eur J Neurol. 2011, 18 (1): 158-164.CrossRefPubMed
29.
go back to reference Wang G, Guo Q, Hossain M, Fazio V, Zeynalov E, Janigro D, Mayberg MR, Namura S: Bone marrow-derived cells are the major source of MMP-9 contributing to blood–brain barrier dysfunction and infarct formation after ischemic stroke in mice. Brain Res. 2009, 1294: 183-192.CrossRefPubMedPubMedCentral Wang G, Guo Q, Hossain M, Fazio V, Zeynalov E, Janigro D, Mayberg MR, Namura S: Bone marrow-derived cells are the major source of MMP-9 contributing to blood–brain barrier dysfunction and infarct formation after ischemic stroke in mice. Brain Res. 2009, 1294: 183-192.CrossRefPubMedPubMedCentral
30.
go back to reference Rosell A, Alvarez-Sabin J, Arenillas JF, Rovira A, Delgado P, Fernandez-Cadenas I, Penalba A, Molina CA, Montaner J: A matrix metalloproteinase protein array reveals a strong relation between MMP-9 and MMP-13 with diffusion-weighted image lesion increase in human stroke. Stroke. 2005, 36 (7): 1415-1420.CrossRefPubMed Rosell A, Alvarez-Sabin J, Arenillas JF, Rovira A, Delgado P, Fernandez-Cadenas I, Penalba A, Molina CA, Montaner J: A matrix metalloproteinase protein array reveals a strong relation between MMP-9 and MMP-13 with diffusion-weighted image lesion increase in human stroke. Stroke. 2005, 36 (7): 1415-1420.CrossRefPubMed
31.
go back to reference Rosell A, Cuadrado E, Ortega-Aznar A, Hernandez-Guillamon M, Lo EH, Montaner J: MMP-9-positive neutrophil infiltration is associated to blood–brain barrier breakdown and basal lamina type IV collagen degradation during hemorrhagic transformation after human ischemic stroke. Stroke. 2008, 39 (4): 1121-1126.CrossRefPubMed Rosell A, Cuadrado E, Ortega-Aznar A, Hernandez-Guillamon M, Lo EH, Montaner J: MMP-9-positive neutrophil infiltration is associated to blood–brain barrier breakdown and basal lamina type IV collagen degradation during hemorrhagic transformation after human ischemic stroke. Stroke. 2008, 39 (4): 1121-1126.CrossRefPubMed
32.
go back to reference Zhou J, Li J, Rosenbaum DM, Barone FC: Thrombopoietin protects the brain and improves sensorimotor functions: reduction of stroke-induced MMP-9 upregulation and blood–brain barrier injury. J Cereb Blood Flow Metab. 2011, 31 (3): 924-933.CrossRefPubMed Zhou J, Li J, Rosenbaum DM, Barone FC: Thrombopoietin protects the brain and improves sensorimotor functions: reduction of stroke-induced MMP-9 upregulation and blood–brain barrier injury. J Cereb Blood Flow Metab. 2011, 31 (3): 924-933.CrossRefPubMed
33.
go back to reference Thiex R: Future perspectives on the fibrinolytic therapy of intracerebral hemorrhages. Cent Nerv Syst Agents Med Chem. 2011, 11 (2): 150-156.CrossRefPubMed Thiex R: Future perspectives on the fibrinolytic therapy of intracerebral hemorrhages. Cent Nerv Syst Agents Med Chem. 2011, 11 (2): 150-156.CrossRefPubMed
34.
go back to reference Wu G, Li S, Wang L, Mao Y: The perihematomal glutamate level is associated with the outcome of patients with basal ganglia hematomas treated by minimally invasive procedures. Neurol Res. 2013, 35 (8): 829-836.CrossRefPubMed Wu G, Li S, Wang L, Mao Y: The perihematomal glutamate level is associated with the outcome of patients with basal ganglia hematomas treated by minimally invasive procedures. Neurol Res. 2013, 35 (8): 829-836.CrossRefPubMed
35.
go back to reference Wu G, Zhong W: Effect of minimally invasive surgery for cerebral hematoma evacuation in different stages on motor evoked potential and thrombin in dog model of intracranial hemorrhage. Neurol Res. 2010, 32 (2): 127-133.CrossRefPubMed Wu G, Zhong W: Effect of minimally invasive surgery for cerebral hematoma evacuation in different stages on motor evoked potential and thrombin in dog model of intracranial hemorrhage. Neurol Res. 2010, 32 (2): 127-133.CrossRefPubMed
Metadata
Title
Effects of minimally invasive procedures for evacuation of intracerebral hematoma in early stages on MMP-9 and BBB permeability in rabbits
Authors
Guofeng Wu
Jing Shi
Fan Wang
Likun Wang
Anrong Feng
Siying Ren
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2014
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/1471-2377-14-85

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